Skip to main content
Log in

Adaptive relationships of epoxide hydrolase in herbivorous arthropods

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Epoxide hydrolase catalyzes a simple hydrolysis of reactive cyclic ethers that may otherwise alkylate and impair critical proteins and nucleic acids required for life. Although much less studied than the cytochrome P-450 monooxygenases that produce epoxides, differences in subcellular, tissue, pH, substrate, and inhibitor specificities argue for at least three forms of insect epoxide hydrolase. Increasing numbers of epoxides are being identified as plant allelochemicals, antifeedants, and essential hormones or precursors for herbivorous arthropods, and in many cases an associated alkene to diol pathway of metabolism is found. A role for epoxide hydrolase in arthropod-plant interactions is strongly supported by species comparisons and by age-activity and induction studies. Two major limitations for study in biochemical ecology of epoxide hydrolase are the lack of an effective in vivo inhibitor and a range of commercially available radiolabeled substrates for the enzymes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ahmad, S. 1986. Enzymatic adaptations of herbivorous insects and mites to phytochemicals.J. Chem. Ecol. 12:533–560.

    Google Scholar 

  • Ahmad, S., Brattsten, L.B., Mullin, C.A., andYu, S. J. 1986. Enzymes involved in the metabolism of plant allelochemicals, pp. 73–151,in L.B. Brattsten and S. Ahmad (eds.). Molecular Aspects of Insect-Plant Associations, Plenum Press, New York.

    Google Scholar 

  • Ajami, A.M., andRiddiford, L.M. 1973. Comparative metabolism of theCecropia juvenile hormone.J. Insect Physiol. 19:635–645.

    Google Scholar 

  • Baars, A.J., Jansen, M., andBreimer, D.D. 1979. Xenobiotic-metabolizing enzymes inDrosophila melanogaster. Activities of epoxide hydratase and glutathioneS-transferase compared with similar activities in rat liver.Mutat. Res. 62:279–291.

    Google Scholar 

  • Banthorpe, D.V., andOsborne, M.J. 1984. Terpene epoxidases and epoxide hydratases from cultures ofJasminum officinale.Phytochemistry 23:905–907.

    Google Scholar 

  • Bell, T.W., andMeinwald, J. 1986. Pheromones of two arctiid moths (Creatonotos transiens andC. gangis): Chiral components from both sexes and achiral female components.J. Chem. Ecol. 12:385–409.

    Google Scholar 

  • Bowers, W.S., andMartinez-Pardo, R. 1977. Antiallatotropins: Inhibition of corpus allatum development.Science 197:1369–1371.

    Google Scholar 

  • Boyland, E. 1950. The biological significance of metabolism of polycyclic compounds.Biochem. Soc. Symp. 5:40–54.

    Google Scholar 

  • Brattsten, L.B. 1979. Ecological significance of mixed-function oxidations.Drug Metab. Rev. 10:35–58.

    Google Scholar 

  • Brattsten, L.B. 1983. Cytochrome P-450 involvement in the interactions between plant terpenes and insect herbivores, pp. 173–195,in P.A. Hedin (ed.). Plant Resistance to Insects, Symp. Ser. No. 208. American Chemical Society, Washington, D.C.

    Google Scholar 

  • Brattsten, L.B., andAhmad, S. (eds.) 1986. Molecular Aspects of Insect-Plant Associations. Plenum Press, New York. 346 pp.

    Google Scholar 

  • Breuer, H., andKnuppen, R. 1961. The formation and hydrolysis of 16α, 17α-epoxyoestratriene-3-ol by the rat liver.Biochim. Biophys. Acta 49:620–621.

    Google Scholar 

  • Brooks, G.T. 1966. Progress in metabolic studies of the cyclodiene insecticides and its relevance to structure-activity correlations.World Rev. Pest Control 5:62–84.

    Google Scholar 

  • Brooks, G.T. 1973. Insect epoxide hydrase inhibition by juvenile hormone analogues and metabolic inhibitors.Nature 245:382–384.

    Google Scholar 

  • Brooks, G.T. 1977. Epoxide hydratase as a modifier of biotransformation and biological activity.Gen. Pharmacol. 8:221–226.

    Google Scholar 

  • Brooks, G.T. 1979. The metabolism of xenobiotics in insects, pp. 151–214,in J.W. Bridges and L.F. Chasseaud (eds.). Progress in Drug Metabolism, Vol. 3. John Wiley, New York.

    Google Scholar 

  • Brooks, G.T., andHarrison, A. 1965. Structure-activity relationships among insecticidal compounds derived from chlordene.Nature 205:1031–1032.

    Google Scholar 

  • Brooks, G.T., Harrison, A., andLewis, S.E. 1970. Cyclodiene epoxide ring hydration by microsomes from mammalian liver and houseflies.Bochem. Pharmacol. 19:225–273.

    Google Scholar 

  • Burnett, W.C., Jr., Jones, S.B., Jr., Mabry, T.J., andPadolina, W.G. 1974. Sesquiterpene lactones—insect feeding deterrents inVernonia.Biochem. Syst. Ecol. 2:25–29.

    Google Scholar 

  • Casida, J.E., andRuzo, L.O. 1986. Reactive intermediates in pesticide metabolism: Peracid oxidations as possible biomimetic models.Xenobiotica 16:1003–1015.

    Google Scholar 

  • Casida, J.E., Kimmel, E.C., Elliott, M., andJanes, N.F. 1971. Oxidative metabolism of pyrethrins in mammals.Nature 230:326–327.

    Google Scholar 

  • Cohen, E. 1981. Epoxide hydrase activity in the flour beetleTribolium castaneum (Coleoptera, Tenebrionidae).Comp. Biochem. Physiol. 69B:29–34.

    Google Scholar 

  • Cohen, E. 1982. Studies on several microsomal enzymes in two strains ofTribolium casteaneum (Tenebrionidae, Coleoptera).Comp. Biochem. Physiol. 71C:123–126.

    Google Scholar 

  • Cova, D., Arnoldi, A., Colombo, R., andRossini, L. 1986. Stereochemical considerations on the inhibition of hepatic epoxide hydrolase by some pesticides and their epoxides.Toxicol. Lett. 30:273–278.

    Google Scholar 

  • Croft, B.A., andMullin, C.A. 1984. Comparison of detoxification enzyme systems inArgyrotaenia citrana (Lepidoptera: Tortricidae) and the ectoparasite,Oncophanes americanus (Hymenoptera: Braconidae).Environ. Entomol. 13:1330–1335.

    Google Scholar 

  • Cross, A.D. 1960. The chemistry of naturally occurring 1,2-epoxidesQt. Rev. Chem. Soc. London 14:317–335.

    Google Scholar 

  • Croteau, R., andKolattukudy, P.E. 1974. Direct evidence for the involvement of epoxide intermediates in the biosynthesis of the C18 family of cutin acids.Arch. Biochem. Biophys. 162:471–480.

    Google Scholar 

  • Dean, F.M. 1963. Naturally Occurring Oxygen Ring Compounds. Butterworths, London.

    Google Scholar 

  • Dowd, P.F., Smith, C.M., andSparks, T.C. 1983. Detoxification of plant toxins by insects.Insect Biochem. 13:453–468.

    Google Scholar 

  • Feyereisen, R., andFarnsworth, D.E. 1987. Precursor supply for insect juvenile hormone III biosynthesis in a cockroach.J. Biol. Chem. 262:2676–2681.

    Google Scholar 

  • Feyereisen, R., Johnson, G., Koener, J., Stay, B., andTobe, S.S. 1981. Precocenes as proallatocidins in adult femaleDiploptera punctata: A functional and ultrastructural study.J. Insect Physiol. 27:855–868.

    Google Scholar 

  • Fitzloff, J.F., andPan, J.C. 1984. Epoxidation of the lindane metabolite, β-PCCH, by human and rat liver microsomes.Xenobiotica 14:599–604.

    Google Scholar 

  • Fox, P.M., andMassare, J.S. 1976. Aspects of juvenile hormone metabolism inPeriplaneta americana (L.).Comp. Biochem. Physiol. 53B:195–200.

    Google Scholar 

  • Fujimoto, Y., Morisaki, M., andIkekawa, N. 1985. Enzymatic dealkylation of phytosterols in insects.Methods Enzymol. 111:346–352.

    Google Scholar 

  • Fukami, J.-I., Yamamoto, I., andCasida, J.E. 1967. Metabolism of rotenone in vitro by tissue homogenates from mammals and insects.Science 155:713–716.

    Google Scholar 

  • Fukami, J.-L., Shishido, T., Fukunaga, K., andCasida, J.E. 1969. Oxidative metabolism of rotenone in mammals, fish, and insects and its relation to selective toxicity.J. Agric. Food Chem. 17:1217–1226.

    Google Scholar 

  • Gadot, M., Goldman, A., Cojocaru, M., andApplebaum, S.W. 1987. The intrinsic synthesis of juvenile hormone-III diol by locust corpora allata in vitro.Mol. Cell. Endocrinol. 49:99–107.

    Google Scholar 

  • Gill, S.S., andHammock, B.D. 1979. Hydration ofcis- andtrans-epoxymethyl stearates by the cytosolic epoxide hydrase of mouse liver.Biochem. Biophys. Res. Commun. 89:965–971.

    Google Scholar 

  • Gold, B., andBrunk, G. 1982. Metabolism of 1,1,1-trichloro-2,2-bis(p-chlorophenyl)ethane and 1,1-dichloro-2,2-bis(p-chlorophenyl)ethane in the mouse.Chem.-Biol. Interact. 41:327–339.

    Google Scholar 

  • Grundy, D.L., andStill, C.C. 1985. Inhibition of acetylcholinesterases by pulegone-1,2-epoxide.Pestic. Biochem. Physiol. 23:383–388.

    Google Scholar 

  • Hallstrom, I., andGrafstrom, R. 1981. The metabolism of drugs and carcinogens in isolated subcellular fractions ofDrosophila melanogaster. II. Enzyme induction and metabolism of benzo[α]pyrene.Chem.-Biol. Interact. 34:145–159.

    Google Scholar 

  • Hammock, B.D. 1985. Regulation of juvenile hormone titer: Degradation, pp. 431–472,in G.A. Kerkut and L.I. Gilbert (eds.). Comprehensive Insect Physiology, Biochemistry and Pharmacology, Vol. 7, Pergamon Press, Oxford.

    Google Scholar 

  • Hammock, B.D., andQuistad, G.B. 1976. The degradative metabolism of juvenoids by insects, pp. 374–393, in L.I. Gilbert (ed.). The Juvenile Hormones. Plenum Press, New York.

    Google Scholar 

  • Hammock, B.D., andQuistad, G.B. 1981. Metabolism and mode of action of juvenile hormone, juvenoids, and other insect growth regulators, pp. 1–83,in D.H. Hutson and T.R. Roberts (eds.). Progress in Pesticide Biochemistry, Vol. 1. John Wiley, New York.

    Google Scholar 

  • Hammock, B.D., Gill, S.S., andCasida, J.E. 1974. Insect metabolism of a phenyl epoxygeranyl ether juvenoid and related compounds.Pestic. Biochem. Physiol. 4:393–406.

    Google Scholar 

  • Hammock, B.D., Nowock, J. Goodman, W., Stamoudis, V., andGilbert, L.I. 1975. The influence of hemolymph-binding protein on juvenile hormone stability and distribution inManduca sexta fat body and imaginai discs in vitro.Mol. Cell. Endocrinol. 3:167–184.

    Google Scholar 

  • Hammock, B.D., Mumby, S.M., andLee, P.W. 1977. Mechanisms of resistance to the juvenoid methoprene in the house flyMusca domestica L.Pestic. Biochem. Physiol. 7:261–272.

    Google Scholar 

  • Hartmann, G.R., andFrear, D.S. 1963. Enzymatic hydration ofcis-9,10-epoxyoctadecanoic acid by cell-free extracts of germinating flax rust uredospores.Biochem. Biophys. Res. Commun. 10:366–372.

    Google Scholar 

  • Hodgson, E. 1985. Microsomal mono-oxygenases, pp. 225–321,in G.A. Kerkut and L.I. Gilbert (eds.). Comprehensive Insect Physiology, Biochemistry and Pharmacology, Vol. 11. Pergamon Press, Oxford.

    Google Scholar 

  • Holloway, P.J., andDeas, A.H.B. 1973. Epoxyoctadecanoic acids in plant cutins and suberins.Phytochemistry 12:1721–1735.

    Google Scholar 

  • Holloway, P.J., Brown, G.A., andWattendorff, J. 1981. Ultrahistochemical detection of epoxides in plant cuticular membranes.J. Exp. Bot. 32:1051–1066.

    Google Scholar 

  • Hsia, M.T.S. 1982–1983. Toxicological significance of dihydrodiol metabolites.J. Toxicol.-Clin. Toxicol. 19:737–758.

    Google Scholar 

  • Hutson, D.H. 1983. Bioactivation involving chemically reactive oxygenated carbon, pp. 263–274,in S. Matsunaka, D.H. Hutson, and S.D. Murphy (eds.). Pesticide Chemistry: Human Welfare and the Environment, Vol. 3 Pergamon Press, Oxford.

    Google Scholar 

  • Jansen, M., Baars, A.J., andBreimer, D.D. 1986. Microsomal and cytosolic epoxide hydrolase inDrosophila melanogaster.Biochem. Pharmacol. 35:2229–2232.

    Google Scholar 

  • Kolattukudy, P.E. 1985. Enzymatic penetration of the plant cuticle by fungal pathogens.Annu. Rev. Phytopathol. 23:223–250.

    Google Scholar 

  • Kramer, S.J., Wieten, M., andDeKort, C.A.D. 1977. Metabolism of juvenile hormone in the Colorado potato beetle,Leptinotarsa decemlineata.Insect Biochem. 7:231–236.

    Google Scholar 

  • Kubo, I., andMatsumoto, T. 1985. Potent insect antifeedants from the African medicinal plantBersama abyssinica, pp. 183–200,in P.A. Hedin (ed.). Bioregulators for Pest Control, Symp. Ser. No. 276. American Chemical Society, Washington, D.C.

    Google Scholar 

  • Kuhr, R.J., andDorough, H.W. 1976. Carbamate Insecticides: Chemistry, Biochemistry and Toxicology. CRC Press, Cleveland, 301 pp.

    Google Scholar 

  • Lu, A.Y.H., andMiwa, G.T. 1980. Molecular properties and biological functions of microsomal epoxide hydrase.Annu. Rev. Pharmacol. Toxicol. 20:513–531.

    Google Scholar 

  • Martin, W.R., andFoster, J.W. 1955. Production oftrans-l-epoxysuccinic acid by fungi and its microbiological conversion tomeso-tartartic acid.J. Bacteriol. 70:405–414.

    Google Scholar 

  • McCord, E., Jr., andYu, S.J. 1987. The mechanisms of carbaryl resistance in the fall armyworm,Spodoptera frugiperda (J.E. Smith).Pestic. Biochem. Physiol. 27:114–122.

    Google Scholar 

  • Miller, T.A., Maynard, M., andKennedy, J.M. 1979. Structure and insecticidal activity of picrotoxinin analogs.Pestic. Biochem. Physiol. 10:128–136.

    Google Scholar 

  • Miranda, C.L., Cheeke, P.R., andBuhler, D.R. 1980. Effect of pyrrolizidine alkaloids from tansy ragwort (Senecio jacobaea) on hepatic drag metabolizing enzymes in male rats.Biochem. Pharmacol. 29:2645–2649.

    Google Scholar 

  • Miyazaki, A., Sakai, M., andMarumo, S. 1979. Comparative metabolism of enantiomers of chlordene and chlordene epoxide in German cockroaches, in relation to their remarkably different insecticidal activity.J. Agric. Food Chem. 27:1403–1405.

    Google Scholar 

  • Mullin, C.A. 1979. Purification and properties of an epoxide hydratase from the midgut of the southern armyworm (Spodoptera eridania). PhD thesis. Cornell University, Ithaca, New York, 231 pp.

    Google Scholar 

  • Mullin, C.A. 1985. Detoxification enzyme relationships in arthropods of differing feeding strategies, pp. 267–278,in P.A. Hedin (ed.). Bioregulators for Pest Control, Symp. Ser. No. 276, American Chemical Society, Washington, D.C.

    Google Scholar 

  • Mullin, C.A. 1986. Adaptive divergence of chewing and sucking arthropods to plant allelochemicals, pp. 175–209,in L.B. Brattsten and S. Ahmad (eds.). Molecular Aspects of Insect-Plant Associations, Plenum Press, New York.

    Google Scholar 

  • Mullin, C.A., andCroft, B.A. 1983. Host-related alterations of detoxification enzymes inTetranychus urticae (Acari: Tetranychidae).Environ. Entomol. 12:1278–1282.

    Google Scholar 

  • Mullin, C.A., andCroft, B.A. 1984.trans-Epoxide hydrolase: A key indicator enzyme for herbivory in arthropods.Experientia 40:176–178.

    Google Scholar 

  • Mullin, C.A., andCroft, B.A. 1985. An update on development of selective pesticides favoring arthropod natural enemies, pp. 123–150,in M.A. Hoy and D.C. Herzog (eds.). Biological Control in Agricultural IPM Systems. Academic Press, New York.

    Google Scholar 

  • Mullin, C.A., andHammock, B.D. 1982. Chalcone oxides—potent selective inhibitors of cytosolic epoxide hydrolase.Arch. Biochem. Biophys. 216:423–439.

    Google Scholar 

  • Mullin, C.A., andWilkinson, C.F. 1980a. Purification of an epoxide hydrolase from the midgut of the southern armyworm (Spodoptera eridania).Insect Biochem. 10:681–691.

    Google Scholar 

  • Mullin, C.A., andWilkinson, C.F. 1980b. Insect epoxide hydrolase: Properties of a purified enzyme from the southern armyworm (Spodoptera eridania).Pestic. Biochem. Physiol. 14:192–207.

    Google Scholar 

  • Mullin, C.A., Croft, B.A., Strickler, K., Matsumura, F., andMiller, J.R. 1982. Detoxification enzyme differences between a herbivorous and predatory mite.Science 217:1270–1272.

    Google Scholar 

  • Mullin, C.A., Matsumura, F., andCroft, B.A. 1984. Epoxide forming and degrading enzymes in the spider mite,Tetranychus urticae.Comp. Biochem. Physiol. 79C:85–92.

    Google Scholar 

  • Nahrstedt, A., Walther, A., andWray, V. 1982. Sarmentosin epoxide, a new cyanogenic compound fromSedum cepaea.Phytochemistry 21:107–110.

    Google Scholar 

  • Nelson, J.O., andMatsumura, F. 1973. Dieldrin (HEOD) metabolism in cockroaches and house flies.Arch. Environ. Contam. Toxicol. 1:224–244.

    Google Scholar 

  • Norris, D.M. 1986. Anti-feeding compounds, pp. 97–146,in G. Haug and H. Hoffman (eds.). Sterol Biosynthesis Inhibitors and Anti-feeding Compounds. Springer-Verlag, New York.

    Google Scholar 

  • Oesch, F. 1973. Mammalian epoxide hydrases: Inducible enzymes catalysing the inactivation of carcinogenic and cytotoxic metabolites derived from aromatic and olefinic compounds.Xenobiotica 3:305–340.

    Google Scholar 

  • Oonnithan, E.S., andMiskus, R. 1964. Metabolism of C14-dieldrin by dieldrin-resistantCulex pipiens quinquefasciatus mosquitoes.J. Econ. Entomol. 57:425–426.

    Google Scholar 

  • Ottea, J.A., andHammock, B.D. 1986. Optimization of assay conditions for epoxide metabolizing enzymes inTrichoplusia ni.Insect Biochem. 16:319–325.

    Google Scholar 

  • Ottea, J.A., Harshman, L.G., andHammock, B.D. 1987a. Patterns of epoxide metabolism by epoxide hydrolase and glutathioneS-transferase associated with age and genotype inDrosophila melanogaster.Muta. Res. 177:247–254.

    Google Scholar 

  • Ottea, J.A., Plapp, F.W., Jr., andHammock, B.D. 1987b. Biochemical and genetic analysis of epoxide metabolizing enzymes in susceptible and resistant house flies,Musca domestica L.Pestic. Biochem. Physiol. 29:138–145.

    Google Scholar 

  • Pratt, G.E., Jennings, R.C., Hamnett, A.F., andBrooks, G.T. 1980. Lethal metabolism of precocene-I to a reactive epoxide by locust corpora allata.Nature 284:320–323.

    Google Scholar 

  • Prestwich, G.D., andBlomquist, G.J. (eds.). 1987. Pheromone Biochemistry. Academic Press, New York, 565 pp.

    Google Scholar 

  • Rees, H.H. 1985. Biosynthesis of ecdysone, pp. 249–293,in G.A. Kerkut and L.I. Gilbert (eds.). Comprehensive Insect Physiology, Biochemistry and Pharmacology, Vol. 7. Pergamon Press, New York.

    Google Scholar 

  • Rothschild, M., Aplin, R.T., Cockrum, P.A., Edgar, J.A., Fairweather, P., andLees, R. 1979. Pyrrolizidine alkaloids in arctiid moths (Lep.) with a discussion on host plant relationships and the role of these secondary plant substances in the Arctiidae.Biol. J. Linn. Soc. 12:305–326.

    Google Scholar 

  • Ruzo, L.O., Casida, J.E., andGammon, D.W. 1984. Neurophysiological activity and toxicity of pyrethroids derived by addition of methylene, sulfur or oxygen to the chrysanthemate 2-methyl-1-propenyl substituent.Pestic. Biochem. Physiol. 21:84–91.

    Google Scholar 

  • Scheune, R.R. 1978. Mammalian Metabolism of Plant Xenobiotics. Academic Press, New York. 502 pp.

    Google Scholar 

  • Schroeder, M.E., Shankland, D.L., andHollinoworth, R.M. 1977. The effects of dieldrin and isomeric aldrin diols on synaptic transmission in the American cockroach and their relevance to the dieldrin poisoning syndrome.Pestic. Biochem. Physiol. 7:403–415.

    Google Scholar 

  • Scott, W.E., Krewson, C.F., Luddy, F.E., andRiemenschneider, R.W. 1963.Vernonia anthelmintica (L.) Willd. enzyme studies. Conversion of epoxyoleic acid to (+)-threo-12,13-dihydroxyoleic acid.J. Am. Oil Chemists' Soc. 40:587–589.

    Google Scholar 

  • Seidegard, J., andDepierre, J.W. 1983. Microsomal epoxide hydrolase. Properties, regulation and function.Biochim. Biophys. Acta 695:251–270.

    Google Scholar 

  • Singh, G.J.P., andSingh, B. 1984. Action of dieldrin andtrans-aidrindiol upon the ultrastructure of the sixth abdominal ganglion ofPeriplaneta americana in relation to their electrophysiological effects.Pestic. Biochem. Physiol. 21:102–126.

    Google Scholar 

  • Slade, M., andWilkinson, C.F. 1973. Juvenile hormone analogs: a possible case of mistaken identity?Science 181:672–674.

    Google Scholar 

  • Slade, M., andWilkinson, C.F. 1974. Degradation and conjugation of Cecropia juvenile hormone by the southern armyworm (Prodenia eridania).Comp. Biochem. Physiol. 49B:99–103.

    Google Scholar 

  • Slade, M., andZibitt, C.H. 1971. Metabolism of Cecropia juvenile hormone in lepidopterans, pp. 45–48,in A.S. Tahori (ed.). Chemical Releasers in Insects, Proc. 2nd IUPAC Congr. Pestic. Chem., Vol. 3. Gordon and Breach, New York.

    Google Scholar 

  • Slade, M., Brooks, G.T., Hetnarski, H.K. andWilkinson, C.F. 1975. Inhibition of the enzymatic hydration of the epoxide HEOM in insects.Pestic. Biochem. Physiol. 5:35–46.

    Google Scholar 

  • Slade, M., Hetnarski, H.K., andWilkinson, C.F. 1976. Epoxide hydrase activity and its relationship to development in the southern armyworm,Prodenia eridania.J. Insect Physiol. 22:619–622.

    Google Scholar 

  • Soderlund, D.M. Messeguer, A., andBowers, W.S. 1980. Precocene II metabolism in insects: Synthesis of potential metabolites and identification of initial in vitro biotransformation products.J. Agric. Food Chem. 28:724–731.

    Google Scholar 

  • Sparks, T.C., andHammock, B.D. 1983. Insect growth regulators: Resistance and the future, pp. 615–668,in G.P. Georghiou and T. Saito (eds.). Pest Resistance to Pesticides. Plenum Press, New York.

    Google Scholar 

  • Tomlin, A.D. 1968.trans-Aldrin glycol as a metabolite of dieldrin in larvae of the southern house mosquito.J. Econ. Entomol. 61:855–857.

    Google Scholar 

  • Tulloch, A.P. 1963. Enzymatic production of (+)-threo-9,10-dihydroxyoctadecanoic acid in the spores of plant rusts.Can. J. Biochem. Physiol. 41:1115–1121.

    Google Scholar 

  • Van Beek, T.A., andDeGroot, A. 1986. Terpenoid antifeedants, parti. An overview of terpenoid antifeedants of natural origin.Recl. Trav. Chim. Pays-Bas 105:513–527.

    Google Scholar 

  • White, R.A., Franklin, R.T., andAgosin, M. 1979. Conversion of α-pinene to α-pinene oxide by rat liver and the bark beetleDendroctonus terebrans microsomal fractions.Pestic Biochem. Physiol. 10:233–242.

    Google Scholar 

  • Wing, K.D., Sparks, T.C., Lovell, V.M., Levinson, S.O., andHammock, B.D. 1981. The distribution of juvenile hormone esterase and its interrelationship with other proteins influencing juvenile hormone metabolism in the cabbage looper,Trichoplusia ni.Insect Biochem. 11:473–485.

    Google Scholar 

  • Wisniewski, J.R., Rudnicka, M., andKochman, M. 1986. Tissue specific juvenile hormone degradation inGalleria mellonella.Insect Biochem. 16:843–849.

    Google Scholar 

  • Wixtrom, R.N., andHammock, B.D. 1985. Membrane-bound and soluble-fraction epoxide hydrolases: Methodological aspects, pp. 1–93,in D. Zakim and D.A. Vessey (eds.). Biochemical Pharmacology and Toxicology, Vol. 1. John Wiley, New York.

    Google Scholar 

  • Yamasaki, R.B., andKlocke, J.A. 1987. Structure-bioactivity relationships of azadirachtin, a potential insect control agent.J. Agric. Food Chem. 35:467–471.

    Google Scholar 

  • Yu, S.J. 1986. Consequences of induction of foreign compound-metabolizing enzymes in insects, pp. 153–174,in L.B. Brattsten and S. Ahmad (eds.). Molecular Aspects of Insect-Plant Associations. Plenum Press, New York.

    Google Scholar 

  • Yu, S.J., 1987. Biochemical defense capacity in the spined soldier bug (Podisus maculiventris) and its lepidopterous prey.Pestic. Biochem. Physiol. 28:216–223.

    Google Scholar 

  • Yu, S.J., andHsu, E.L. 1985. Induction of hydrolases by allelochemicals and host plants in fall armyworm (Lepidoptera: Noctuidae) larvae.Environ. Entomol. 14:512–515.

    Google Scholar 

  • Yu, S.J., andTerriere, L.C. 1978a. Metabolism of juvenile hormone I by microsomal oxidases, esterase, and epoxide hydrase ofMusca domestica and some comparisons withPhormia regina andSarcophaga bullata.Pestic. Biochem. Physiol. 9:237–246.

    Google Scholar 

  • Yu, S.J., andTerriere, L.C. 1978b. Juvenile hormone epoxide hydrase in house flies, flesh flies and blow flies.Insect Biochem. 8:349–352.

    Google Scholar 

  • Yu, S.J., Robinson, F.A., andNation, J.L. 1984. Detoxication capacity in the honey bee,Apis mellifera L.Pestic. Biochem. Physiol. 22:360–368.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mullin, C.A. Adaptive relationships of epoxide hydrolase in herbivorous arthropods. J Chem Ecol 14, 1867–1888 (1988). https://doi.org/10.1007/BF01013483

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01013483

Key words

Navigation